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Peritoneal Metastases: Detection with Spiral CT in Patients with Ovarian Cancer¹

¹ From the Departments of Radiology (F.V.C., P.H.C., C.A.G., H.H.), Epidemiology and Biostatistics (E.V.), and Surgery (B.P., D.C.), Memorial Sloan-Kettering Cancer Center, New York, NY; and the Institution of Oncology, Radiology, and Clinical Immunology, Section of Radiology, University Hospital, Uppsala, Sweden (A.B.). Received June 22, 2001; revision requested August 2; revision received September 25; accepted October 22. Address correspondence to F.V.C., Department of Radiology, University of California, San Francisco, 505 Parnassus Ave, Box 0628, M-372, San Francisco, CA 94143-0628 (e-mail: fergus.coakley@radiology.ucsf.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To determine the accuracy of spiral computed tomography (CT) in the depiction of peritoneal metastases by using surgical findings in patients with ovarian cancer as the standard of reference.

MATERIALS AND METHODS: Three independent readers reviewed the preoperative CT scans obtained in 64 patients who underwent primary surgery for ovarian cancer. Readers rated the likelihood of peritoneal metastases on a five-point scale and recorded the presence or absence of ascites, parietal peritoneal thickening or enhancement, and small-bowel wall thickening or distortion. Peritoneal metastases were identified as nodular, plaquelike, or infiltrative soft-tissue lesions in the peritoneal fat or on the peritoneal surface. Area under the receiver operating characteristic curve was calculated for each reader. Interreader agreement was evaluated with the statistic. Descriptive statistical data were determined with dichotomized ratings (1–3 = absent; 4–5 = present).

RESULTS: Areas under the receiver operating characteristic curves for the three readers were 0.95, 0.93, and 0.89. Paired values ranged from 0.75 to 0.91. Reader sensitivity for metastases 1 cm or smaller in maximum diameter (25%–50%) was significantly (P < .05) lower than overall sensitivity (85%–93%). Ascites, parietal peritoneal thickening or enhancement, and small-bowel wall thickening or distortion demonstrated positive predictive values of 72%–93%, with values of 0.12–0.80.

CONCLUSION: Spiral CT is accurate in the depiction of peritoneal metastases from ovarian cancer, although sensitivity is reduced in patients with tumor implants 1 cm or smaller. Ancillary signs of peritoneal malignancy are limited by low interobserver agreement.

© RSNA, 2002

Index terms: Computed tomography (CT), helical, 791.33, 852.12115 • Ovary, neoplasms, 852.32, 852.33 • Peritoneum, CT, 791.12112, 791.12115 • Peritoneum, neoplasms, 791.33

	INTRODUCTION

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The peritoneal cavity is a common site of metastatic spread for many malignancies. For example, approximately 71%, 17%, and 10% of patients with ovarian, gastric, and colorectal cancer, respectively, have peritoneal metastases at the time of initial presentation (1–3). Peritoneal metastases are an important cause of morbidity and mortality. A review (4) of several studies involving patients with a variety of underlying primary tumors showed the median survival after a diagnosis of malignant ascites was 1–8 months. The median survival of patients with peritoneal metastases from colorectal cancer is 9 months (5).

Authors of previous studies (1,6,7) in which the accuracy of computed tomography (CT) in the diagnosis of peritoneal metastases was examined have reported a sensitivity of 63%–79% and a specificity of 100%. We hypothesize that sensitivity may have improved since these studies were performed because of improvements in CT technology and greater awareness of imaging findings in peritoneal disease (8). In particular, the absence of section misregistration artifact at spiral CT should help in the distinction of unopacified bowel loops from tumor implants (6). Studies in which the CT depiction of peritoneal metastases is investigated are frequently conducted with patients who have ovarian cancer because surgery is the standard of care in most cases of ovarian malignancy, irrespective of stage. Studies in patients with peritoneal metastases from other primary tumors in which surgical findings are used as the standard of reference are subject to potential verification bias because the preoperative detection of peritoneal metastases may be a contraindication to surgery. The purpose of our study was to determine the accuracy of spiral CT in the depiction of peritoneal metastases by using surgical findings in patients with ovarian cancer as the standard of reference.

	MATERIALS AND METHODS

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Subjects
By means of a computerized review of the surgical records at our institution (Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY), 300 patients who underwent primary surgery for histopathologically confirmed ovarian cancer between June 1996 and August 2000 were identified. Patients who did not have preoperative spiral CT scans of the abdomen and pelvis available for review were excluded (n = 234); many patients underwent CT at outside institutions, and these studies were frequently unavailable. The remaining 64 patients formed the study population. In this group, the mean patient age was 55 years (age range, 28–81 years), and the mean interval from CT to surgery was 14 days (range, 0–42 days). The study was approved by our institutional review board; informed consent was not required.

CT Technique
All CT examinations were performed with spiral scanners, whether conducted at our institution (n = 24) or at other institutions (n = 40). All scans were obtained from the diaphragm to the ischial tuberosities. At our institution, CT scans were obtained with a high-speed scanner (CT HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis). The type of scanner used at the other institutions was unknown. All CT scanning examinations were performed after oral administration of contrast material, and in 62 of 64 patients, scanning was performed after intravenous administration of contrast material. All scans were obtained spirally, with a section collimation of 5 mm (n = 3), 7–8 mm (n = 39), or 10 mm (n = 22). At our institution, CT scans were obtained with a pitch of 1 during two suspended respirations after intravenous administration of 150 mL of nonionic contrast material at a rate of 2.5 mL/sec.

Image Analysis
Three attending radiologists (F.V.C., P.H.C., C.A.G.) who had subspecialist expertise in oncologic imaging and who were unaware of the clinical or pathologic findings independently reviewed the CT scans. They rated the likelihood of peritoneal metastases outside the true pelvis on a five-point scale as follows: 1, definitely absent; 2, probably absent; 3, indeterminate; 4, probably present; and 5, definitely present. All three readers used the same criteria for the identification of a peritoneal metastasis, namely, the presence of a nodular, plaquelike, or infiltrative soft-tissue lesion in the peritoneal fat or on the peritoneal surface (1,6). We tailored the study to the detection of extrapelvic peritoneal metastases because of the difficulty in distinguishing large primary tumors in the pelvis from adjacent direct contiguous tumor spread or implants. Readers also recorded the presence or absence of ascites, parietal peritoneal thickening or enhancement, and small-bowel wall thickening or distortion, since these have been described as ancillary signs of peritoneal malignancy (9).

Standard of Reference
The presence or absence of extrapelvic peritoneal metastases was established with staging laparotomy in all patients, in accordance with the International Federation of Obstetrics and Gynecology surgical staging system for ovarian cancer (10). Fourteen (22%) of 64 patients had tumor confined to the ovary (stage I). Five patients (8%) had disease extension or peritoneal metastases confined to the true pelvis (stage II). Thirty-three patients (52%) had extrapelvic peritoneal metastases or abdominopelvic nodal metastases without more distant disease (stage III). Twelve patients (19%) had metastases outside of the peritoneal cavity or abdominopelvic nodes (stage IV). Four of the 45 patients with advanced disease (stages III and IV) had abdominopelvic nodal metastases (n = 3) or distant metastases (n = 1) in the absence of extrapelvic peritoneal metastases. Accordingly, 41 patients had extrapelvic peritoneal metastases.

All cases of peritoneal spread were confirmed with surgical findings and histologic review of omentectomy, debulking, or biopsy specimens. Final histopathologic analysis of the primary tumors demonstrated epithelial ovarian cancer (n = 56), ovarian tumor of low malignant potential (n = 5), malignant müllerian tumor (n = 2), and immature teratoma (n = 1). The epithelial cancers were subtyped as serous (n = 26), endometrioid (n = 14), mucinous (n = 6), mixed (n = 5), clear cell (n = 4), and undifferentiated (n = 1). To investigate the effect of implant size on CT accuracy, we also recorded the maximum diameter of the largest extrapelvic implant as noted at surgery.

Data Analysis
Reader interpretations were compared with the surgical and histopathologic standard of reference. Area under the receiver operating characteristic curve was calculated for each reader, and the significance of observed differences was determined with permutation tests. A P value less than .05 was considered to indicate a statistically significant difference. Interreader agreement was evaluated with the statistic. Descriptive statistical data—specifically, sensitivity, specificity, positive predictive value, and negative predictive value—were determined with dichotomized ratings (1–3 = absent; 4–5 = present).

To investigate the effect of implant size on reader performance, we examined reader accuracy in the subgroup of patients without implants or with implants 1 cm or smaller in maximum diameter. Ascites, parietal peritoneal thickening or enhancement, and small-bowel wall thickening or distortion were analyzed for discriminative value and objectivity in the diagnosis of peritoneal malignancy by means of calculating descriptive statistical data and paired values. The degree of observer agreement as indicated by values was interpreted as follows: 0–0.20, slight agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, substantial agreement; and 0.81–1.00, almost perfect agreement (11).

	RESULTS

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Forty-one (64%) of 64 patients had extrapelvic peritoneal metastases. The areas under the receiver operating characteristic curve for the three readers were 0.95, 0.93, and 0.89 (Fig 1). Paired values ranged from 0.75 to 0.91. Reader performance measurements are listed in Table 1 and are based on dichotomized ratings. Reader performance measurements for the detection of peritoneal metastases in patients without implants or with implants 1 cm or smaller in maximum diameter are shown in Table 2. Reader sensitivity (25%–50%) was significantly (P < .05) lower for the detection of peritoneal metastases in patients with implants 1 cm or smaller in maximum diameter, as compared with reader sensitivity for the detection of peritoneal metastases in all patients (85%–93%). A representative example of a small implant detected by all readers is shown in Figure 2. Positive predictive values for the three readers were 88%–97%, and false-positive findings were unusual (Fig 3). Reader performance measurements for the ancillary signs of peritoneal malignancy are shown in Table 3, and values for interobserver agreement are listed in Table 4.

View larger version (29K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Graph shows receiver operating characteristic curves for the detection of peritoneal metastases in patients with ovarian cancer on spiral CT scans interpreted by three independent readers. AUC = area under the curve.

View larger version (127K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Transverse preoperative contrast material-enhanced CT scan obtained in 61-year-old woman with mixed endometrioid and papillary serous adenocarcinoma of the ovary shows peritoneal implant (arrow) adjacent to the descending colon. All readers detected this implant. Inspection of adjacent sections (not shown) showed the lesion did not represent partial volume averaging with adjacent bowel loops.

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Transverse preoperative contrast-enhanced CT scan obtained in 50-year-old woman with mixed endometrioid and mucinous adenocarcinoma of the ovary shows apparent nodularity (arrows) in the paracolic gutters. All readers interpreted these findings as highly suggestive of peritoneal metastases, but no tumor implants were found at surgery. The pathologic basis of the CT appearance in this case is unknown.

	DISCUSSION

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The introduction of spiral CT does not seem to have greatly improved sensitivity for the detection of smaller implants. Authors of prior studies (1,7) of conventional CT in which a size threshold of 5 mm in diameter was used reported a sensitivity of 28%–51% for the detection of smaller implants. The intraperitoneal use of contrast material or the use of contrast-enhanced magnetic resonance imaging may help in the detection of smaller or equivocal implants (6,12–14), but miliary metastases are likely to continue to elude imaging visualization with current technology. Therefore, a positive imaging-based diagnosis of peritoneal metastases remains clinically more useful than a negative result. The imaging-based diagnosis of peritoneal malignancy in a patient undergoing preoperative staging can enable diagnostic confirmation with percutaneous biopsy or laparoscopy (15,16), and the patient may be spared the complications associated with laparotomy. Ovarian cancer is an exception, because the detection of peritoneal metastases is not of itself a contraindication to curative surgery; rather, tumor debulking is considered the optimal treatment in the majority of these patients.

We are aware of two studies in which spiral CT scanners were used to investigate the detection of peritoneal metastases. Low et al (13) reported a sensitivity of only 51% (21/41) for the detection of peritoneal, omental, and mesenteric disease sites by means of spiral CT with 8–10-mm collimation in a group of patients with extrahepatic abdominal malignancies. However, the authors of this study used data from the initial radiology reports issued by a variety of readers and did not analyze the results according to lesion size. Tempany et al (17) reported a sensitivity of 92% (46/50) for the detection of peritoneal metastases by means of CT in which a protocol with 5-mm sections at 8–10-mm intervals was used in patients with ovarian cancer.

Like other investigators, we observed a high specificity and positive predictive value for the diagnosis of peritoneal metastases. This finding presumably reflects the fact that noncancerous mimics of peritoneal malignancy are rare. Such mimics include tuberculous peritonitis, mesenteric panniculitis, leiomyomatosis peritonealis disseminata, extramedullary hematopoiesis, and chronic leak from an ovarian dermoid cyst with granulomatous peritonitis (18–22). None of these conditions was present in the patients in our study. Despite this, there was one CT study that was interpreted by all readers as highly suggestive of peritoneal metastases (Fig 3); however, no peritoneal metastases were found at surgery. The basis of the CT findings in this case is unknown. It is theoretically possible that small-volume disease may be overlooked at surgery, and this suggests that patient outcome rather than surgical findings may ultimately be a more desirable standard of reference for imaging studies.

The ancillary signs of peritoneal malignancy were investigated in a previous retrospective study (9) involving 60 patients with proved peritoneal metastases from a variety of primary cancers. Ascites, parietal peritoneal thickening or enhancement, and small-bowel wall thickening or distortion were described in 74%, 62%, and 36% of cases, respectively. This study had several features that made it difficult to evaluate the usefulness of these secondary signs. The method by which the signs were assessed was not described, interobserver agreement was not reported, and specificity could not be evaluated because only patients with peritoneal metastases were included.

Our results address some of these issues. We found the presence of ascites to be a reasonably predictive (positive predictive value of 72%–80%), sensitive (sensitivity of 76%–88%), and objective ( values of 0.64–0.80) sign of peritoneal metastases in the patient group in our study. However, while parietal peritoneal thickening or enhancement and small-bowel wall thickening or distortion were predictive of peritoneal metastases (positive predictive values of 80%–93%), both of these signs were limited by poor sensitivity (sensitivity of 12%–68%) and objectivity ( values of 0.12–0.50). We suspect this reflects the inherent lack of specificity and objectivity of these signs, which lack a clear definition and are often based on subjective evaluation.

Our study had a number of limitations. First, the inclusion of patients with only ovarian cancer represents a potentially important source of selection bias, so our results may not be applicable to the detection of peritoneal metastases from other primary malignancies. However, a study (2) of spiral CT in the preoperative staging of gastric cancer demonstrated a sensitivity of 71% (12 of 17) for the detection of peritoneal metastases. The similarity of this result to the sensitivity in our study suggests that our results may be representative of the performance of CT in the depiction of peritoneal metastases from nonovarian cancers.

Second, we performed our analysis on a per patient rather than per nodule basis, and, therefore, we cannot determine the site-by-site accuracy of CT in the depiction of peritoneal implants. We chose this method because accurate correlation of small nodules is impractical, particularly in a retrospective review. In addition, for most cancers, the diagnosis of peritoneal spread is the critical observation, and the distribution of peritoneal implants is of lesser importance.

Third, this study included CT scans obtained by using varying CT techniques at different institutions. For example, 34% (22 of 64) of the CT scans in our study were obtained with 10-mm collimation, which may partially account for the limited sensitivity in the detection of implants 1 cm or smaller.

In conclusion, spiral CT is accurate in the depiction of peritoneal metastases from ovarian cancer, although sensitivity is reduced for tumor implants 1 cm or smaller in maximum diameter, and ancillary signs of peritoneal malignancy are limited by relatively low interobserver agreement.

	FOOTNOTES

 
Author contributions: Guarantors of integrity of entire study, F.V.C., H.H.; study concepts, F.V.C., H.H.; study design, F.V.C., C.A.G.; literature research, F.V.C.; clinical studies, F.V.C., C.A.G., P.H.C., A.B.; data acquisition, F.V.C., C.A.G., P.H.C.; data analysis/interpretation, E.V.; statistical analysis, E.V.; manuscript preparation, F.V.C., D.C., B.P.; manuscript definition of intellectual content, F.V.C., H.H.; manuscript editing, revision/review, and final version approval, all authors.

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Coakley, F. V. Articles by Hricak, H. Search for Related Content PubMed PubMed Citation Articles by Coakley, F. V. Articles by Hricak, H.